Upload
others
View
2
Download
0
Embed Size (px)
Citation preview
Mailing address: Niklas Björklund, Dept. of Ecology, Box 7044 /
Johanna Boberg, Dept. of Forest Mycology and Plant Pathology,
Box 7026, SLU, 750 07 Uppsala
E-mail / Phone:
Street address: Ulls Väg 16 / Almas Allé 5, Uppsala
Org nr: 202100-2817
www.slu.se
[email protected], +46 (0)18-67 28 79
[email protected], +46 (0)18- 67 18 04
Unit for Risk Assessment of Plant Pests REPORT SLU ua 2018.2.6-1762
21/9/2018
Synchytrium endobioticum – pathotypes, resistance of
Solanum tuberosum and management
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
2/23
Content
Summary .................................................................................................................... 3
Background and assignment ...................................................................................... 4
Description of Synchytrium endobioticum................................................................. 4
Life cycle .............................................................................................................. 4
Geographical distribution ..................................................................................... 5
Different pathotypes ............................................................................................. 5
Synchytrium endobioticum in Sweden .................................................................. 7
Genetic components of virulence ......................................................................... 8
Recent progress of detection and diagnostic methods .......................................... 9
Resistance in potato against different pathotypes .................................................... 11
Genetic components of resistance ...................................................................... 11
Breeding and resistant potato cultivars ............................................................... 12
Management options and perspectives .................................................................... 13
Epidemiology and management ......................................................................... 13
Resistant potato cultivars and Council Directive 69/464/EEC ........................... 14
Descheduling of previously infected fields ........................................................ 17
Authors .................................................................................................................... 18
References................................................................................................................ 19
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
3/23
Summary
Synchytrium endobioticum is the causal agent of potato wart. This quarantine
potato pathogen is believed to originate in the Andean mountains of Latin America
and spread to Europe and further to other parts of world at the end of the nineteenth
century. The pathogen is found as different pathotypes displaying differences in
virulence against different potato cultivars. Currently around 40 different
pathotypes have been described in Europe. There is no clear relationship between
pathotypes and genotypes and therefore isolates of the pathogen with different
genotypes and origin can still display the same virulence profile in bioassays.
Several collaborative research initiatives have been undertaken and the detection
and diagnostics methods available has been improved and updated. However, the
EPPO standard bioassay available to describe the different pathotypes is limited to
the detection of the major pathotypes 1(D1), 2(G1), 6(O1) and 18(T1). There is
currently no agreed standard assay available to detect and describe other
pathotypes.
The resistance breeding is complicated by the complex inheritance pattern of
cultivated potato and that different genes and different alleles are involved in the
resistance against different pathotypes. Nevertheless breeding for resistance in
potato has been very successful against pathotype 1(D1). However, it has proven
more difficult against the other pathotypes. Fewer potato cultivars that are resistant
against e.g. pathotypes 2(G1), 6(O1) and 18(T1) are thus available and even fewer
for the more rarely found pathotypes.
S. endobioticum is extremely resistant and the only efficient way to control the
disease is to prevent the spread into new locations. The use of resistant potato
cultivars is an essential part of the current control strategy to limit further spread.
The level of resistance required to prevent further spread is however not known
and no standard is currently available for the assessment of the level of resistance
of different potato cultivars, although it is under development at EPPO. The level
of resistance of the potato cultivars used is not only important in terms of
preventing secondary spread of the pathogen but has also been found to affect the
potential for development of new pathotypes.
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
4/23
Background and assignment
In 2017, pathotype 8(F1) and 40(BN1) of the quarantine pathogen Synchytrium
endobioticum, which is the causal agent of potato wart, were found for the first
time in Sweden (Swedish Board of Agriculture, 2018). Due to these findings the
Swedish Board of Agriculture requested the Unit for Risk Assessment of Plant
Pests at SLU to conduct a review of the available information in order to describe;
the different pathotypes of S. endobioticum in Europe, the corresponding resistance
found in different potato cultivars, and the potential consequences of the currently
used management practises. Furthermore, the recent progress in the work to
harmonise diagnostic methods across Europe and the development of molecular
detection methods was summarised.
This final report replaces the interim report delivered May 21, 2018.
Description of Synchytrium endobioticum
Life cycle
Synchytrium endobioticum is an obligate biotrophic chytrid fungus, i.e. it is a
species that is dependent on live hosts and belongs to a basal lineage in the fungal
kingdom. It lacks hyphae and instead is characterized by the production of mobile
zoospores and the development of long-lived sporangia. The fungus has two
reproductive cycles (Franc, 2007). It has an asexual reproduction cycle with the
production of summer sporangia and release of infectious zoospores during
conducive conditions (spring and summer). The fungus also has a sexual
reproduction cycle, which is initiated during unfavourable conditions (autumn and
winter), where zoospore-like gametes fuse, infect the host and develop into resting
or winter sporangia.
In short, the different stages in the life cycle are as follows (Weiss 1925; Hampson
1993; Franc 2007 and references therein); after winter when the environmental
conditions become favourable (>8C and high water content), zoospores are
released from overwintering resting sporangia. The zoospores swim in the water
film in the soil and infect the potato tuber or stolon. Infected epidermal cells starts
to swell and the zoospore develops into an aggregate structure containing several
zoosporangia known as a sorus. Each sporangium gives rise to hundreds of new
haploid zoospores released into the soil water to further infect susceptible host
tissue. This asexual reproductive cycle continues as long as the conditions are
favourable. Each cycle takes about 10-12 days (Weiss, 1925).
When environmental conditions become unfavourable (e.g. dry or cold) a sexual
reproduction cycle is initiated. The different segments of the sorus then produce
gametes that resemble zoospores but are smaller in size. These gametes may fuse,
forming diploid zygotes that can swim to infect a host cell. The infection develops
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
5/23
into a resting sporangium which is released into the soil as the host tissue decay
(Franc, 2007). Germination of the resting sporangia is possible within two months
but the sporangium may also remain dormant to overwinter (Weiss, 1925). The
resting sporangia are extremely resistant and can survive more than 40 years in the
soil (Przetakiewicz, 2015a).
Geographical distribution
Synchytrium endobioticum is believed to originate in the Andean mountains of
Latin America where it probably co-evolved with potato (Hampson, 1993). At the
end of the nineteenth century it spread to Europe and parts of North America and
further to potato-growing countries in Asia, Africa and Oceania (Hampson 1993;
Baayen et al., 2006). Recent studies show that the pathogen has been introduced to
Europe at least three times (Van de Vossenberg et al. 2018a).
Following the introduction to Europe the pathogen caused outbreaks in many
European countries (Hampson 1993). Today, the pathogen has been reported from
most countries in Europe, although it has been eradicated in some of them (EPPO,
2018a). The distribution is fragmented and localised, probably as a result of the
strict regulatory strategies in place (Obidiegwu et al. 2014).
Different pathotypes
Synchytrium endobioticum is found in different variants displaying differences in
virulence against different potato cultivars classified as different pathotypes, also
referred to as different races. A standard differential set of potato cultivars is used
in bioassays to define the four major pathotypes, i.e. 1(D1), 2(G1), 6(O1) and
18(T1) (Baayen et al. 2006; EPPO 2017a). To define other pathotypes other
cultivars needs to be added to the bioassay.
For a long time the first pathotype described, 1(D1), was the only one found in
Europe (Baayen et al. 2006). However, in the early 1940’s many new pathotypes
were discovered as symptoms developed on formerly resistant potato cultivars
(Baayen et al. 2006). Currently, around 40 different pathotypes have been
described in Europe, but some has not been found for many years and others are
considered to be of minor importance (Table 1)(Baayen et al. 2006; Cakir et al.
2009; Przetakiewicz 2015b). New pathotypes are, nevertheless, still reported, e.g.
the pathotype 38(Nev) and 39(P1) found in Turkey and Poland, respectively,
(Cakir et al. 2009; Przetakiewicz 2015b).
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
6/23
Table 1. Described pathotypes of Synchytrium endobioticum, their importance and
reported distribution, i.e. presence in different countries. The information is mainly
based on the summary table provided in Baayen et al. (2006) but additional
information has been added from other sources.
Pathotype Importance Distribution Referencesd
1 (D1) + multinational 1
2 (G1)a + Germany, The Netherlands,
Czech Republic, Canada, Turkey
1; 2
2(Ch1) + Poland 1; 3; 4
3(SB) Eradicated Czech Republic, Canada 1
3(M1) + Poland 3; 4; 12
4(P1), 5(K1), 7(S1), 9(R1), 10(E1),
12(B1)
Eradicated Germany 1
6(O1)b + Germany, The Netherlands,
Czech Republic, Canada, Turkey
1; 5
8(F1) + Germany, Canada, Sweden,
Bulgaria, Denmark
1; 6; 7; 8
14(Newfoundland) - Canada 1
15(P2), 16(N1), 17(M2), 26(S3),
27(MS1)
+ Czech Republic 1
19(V1), 23(NR1), 24(R3), 28(T2),
29(K2), 30(M3), 31(OL1), 32(V2),
33(K3)
34(K4), 35(L1), 36(ZZ1), 37(K5)
- Czech Republic 1
11(M1), 13(R2), 16(Sinevik),
18(Yasinya), 20(Sheshory),
21(Sokolovka), 22(Bystrets)
+ Ukraine 1
18(T1) + Germany, The Netherlands,
Sweden, Turkey, Poland, Greece
1; 5; 9; 14
38(Nev) ? Turkey 5; 10
39(P1) + Poland 11; 12
40 (BN1)c ? Poland, Sweden 4; 13
aIncluding a pathotype earlier described as 19(Haag) (Baayen et al. 2006). bIncluding a pathotype earlier described as 20(Innernzell) (Baayen et al. 2006). cThe virulence profile of this pathotype has not yet been published. dReferences: (1) Baayen et al. 2006, (2) Cakir & Demirci 2017, (3) Przetakiewicz 2010, (4) European
Commission 2014, (5) Cakir et al. 2009, (6) Busse et al. 2017, (7) Nielsen, 2017, (8) Laginova 2017, (9)
Przetakiewicz 2014, (10) Cakir 2005, (11) Przetakiewicz 2015b, (12) Plich et al. 2018, (13) Swedish Board of
Agriculture, 2018 and (14) van de Vossenberg et al. 2018a.
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
7/23
The pathotypes 1(D1), 2(G1), 6(O1), and 18(T1) are considered to be the most
widespread and important pathotypes in the western part of the EPPO region
(EPPO, 2017a). These are also the pathotypes included in the EPPO standard
(EPPO, 2017a), i.e. the only pathotypes that can be distinguished from each other
based on the susceptibility of the set of differential potato cultivars in the EPPO
standard. There are nevertheless also other pathotypes with a more limited
distribution that potentially are economically important, e.g. 2(Ch1) and 3(M1) in
Poland (Plich et al. 2018).
Synchytrium endobioticum in Sweden
In Sweden, the first observation of the potato wart disease was made in 1912 on
potato from a garden plot on Ljusterön in Stockholm County (Hammarlund, 1915).
Tracing the origin of the seed potatoes used led to further findings of infected fields
in Södermanland County. Hammarlund (1915) arrived to the conclusion that the
disease arrived during the years 1910-1911, most likely from Germany.
Only pathotype 1(D1) had been reported until 2004 when a second pathotype
18(T1) was found (Nordin and Kvist, 2008). Then in 2017, two new isolates
displaying the resistant pattern corresponding to those of pathotype 8(F1) and
40(BN1) were found (Swedish Board of Agriculture, 2018). While isolates of
pathotype 1(D1) has been found in locations ranging from the most southern part
of Sweden up to the provinces of Dalarna and Hälsingland (Melin and Nordin,
1996), the distribution of the findings of other pathotypes are restricted to a much
smaller region between the eastern parts of Skåne and western part of Blekinge
(Swedish Board of Agriculture, 2018).
Here follows a short description of each of the four pathotypes which has been
found in Sweden:
Pathotype 1(D1) has a multinational distribution but the current impact of
pathotype 1(D1) has been questioned and in Germany, for example, pathotype
1(D1) is responsible for less than 1% of all outbreaks (Schlenzig 2008). Breeding
for resistance against this pathotype was very successful and this created an
abundance of potato cultivars resistant to pathotype 1(D1) which effectively
controlled the disease (Baayen et al. 2006). Due to extensive use of resistant potato
cultivars, Baayen et al. (2005) considers pathotype 1(D1) to be eradicated in most
European countries.
Pathotype 18(T1) is also reported from Germany, the Netherlands, Turkey, Poland
and Greece (Baayen et al. 2006; Cakir et al. 2009; Przetakiewicz 2014; van de
Vossenberg et al. 2018a). The pathotype was first described in Germany in the
1970’s (Stachewicz 1978). It is considered to be more virulent than other
pathotypes (Busse et al. 2017).
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
8/23
Pathotype 8(F1) is considered to be important, has previously been reported from
Germany, Canada (Newfoundland), Denmark, and it has probably also recently
been found in Bulgaria (Baayen et al. 2006; Nielsen, 2017; Laginova 2017). It has
however caused less damage than the other main pathotypes, i.e. pathotypes 2(G1),
6(O1) and 18(T1) (Nielsen (2017) citing personal communication with Flath in
2017). There is currently a discussion about pathotype 8(F1) among the institutions
that perform diagnostics since the pathotypes 8(F1) and 18(T1) display very similar
virulence pattern (Nielsen 2017). In the EPPO-standard from 2003 pathotype 8(F1)
was included but in the revised 2017 version it is stated that ”In particular, it should
be noted that pathotype 8(F1) has not been included in the table as distinction from
pathotype 18(T1) is difficult. In case of doubt, specialist laboratories should be
contacted (see section 8, Further information).”. From a practical point of view, it
has been questioned whether it is relevant to distinguish pathotype 8(F1) from
pathotype 18(T1). Pathotype 8(F1) is not included in the official tests that are done
in the Netherlands and in Germany they stopped testing for pathotype 8(F1) when
pathotype 18(T1) was found there (Nielsen (2017) citing personal communication
with Flath in 2017).
Pathotype 40(BN1) is a new pathotype for which the virulence profile has not yet
been published. It was first found in Poland in 2010 and later, in the same region as
the first finding, both in 2011 and 2012 (European Commission, 2014). The
pathotype is reported to be present to a limited extent in the southern parts of
Poland (European Commission, 2014). The identification of this pathotype,
requires additionally differential potato cultivars to be included in the bioassay, in
addition to the standard set included in the EPPO standard (EPPO 2017a). If the
bioassay is performed using the differential potato cultivars included in the EPPO
standards (EPPO, 2004; EPPO, 2017a), the resulting virulence profile of isolates of
pathotype 40(NB1) appear to match that of other pathotypes (Fitopatologii 2016).
Genetic components of virulence
Few studies have been conducted to unravel the genetic components for virulence
in S. endobioticum. The difficulty of obtaining pure cultures on artificial media due
to S. endobioticum being an obligate biotroph may be one main reason (Obidiegwu
et al. 2014; Bonants et al. 2015). Consequently the knowledge about the genetic
basis for virulence of the pathogen and the genetic difference between the
pathotypes is limited. Nevertheless, recent studies conducted with the aim to
develop molecular methods to differentiate between pathotypes and to determine
the intraspecific variation of the pathogen has provided some insights.
In a recent study the DNA of several pathotypes of S. endobioticum was sequenced
and revealed tree distinct genotype groups (Busse et al. 2017). The pathotypes
1(D1), 39(P1) and 2(Ch1) was classified into one group, pathotypes 2(G1), 3(M1)
and 6(O1) formed a second group, while 8(F1) and 18(T1) were classified together
into a third group (Busse et al. 2017).
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
9/23
The different pathotypes appear to be genotypically very similar to each other and
the development of new pathotypes has been suggested to most likely arise from
small changes in avirulence factors, i.e. molecules involved in the host-pathogen
interaction, rather than through recombinations of divergent genotypes (Bonants et
al. 2015; Busse et al. 2017). Still, genetic variation has been found among isolates
of pathotype 1(D1) (Bonants et al. 2015). Some isolates of pathotype 1(D1) from
Sweden and United Kingdom for example appear to lack a genetic marker found in
isolates from Germany and the Netherlands (Bonants et al. 2015; EPPO 2017a; van
de Vossenberg et al. 2018b).
Recent studies on the intraspecific variation of the pathogen have shown that there
are in fact clear genotypic differences between isolates within the S. endobioticum
community. Gagnon et al. (2016) found that European isolates included in the
study were genetically different and did not cluster according to geographical
origin of the isolates. This is corroborated by Van de Vossenberg et al. (2018a) that
investigated the population dynamics by studying the mitochondrial genome of the
pathogen.
Both studies further indicate that there is no clear association between the
genotypes and the pathotypes (Gagnon et al. 2016; van de Vossenberg et al.
2018a). In the study by van de Vossenberg et al. (2018a), the pathotypes 2(G1),
6(O1) and 8(F1) were found in different mitochondrial lineages. That is, the same
pathotype was derived within different mitochondrial groups or, in other words,
isolates of the pathogen with different genotypes and origin can still display the
same virulence profile. Although this observation may be the results of selective
processes it may also be partly ascribed to the difficulty of determining the
virulence profile using bioassays (Gagnon et al. 2016). Linked to the recent finding
of pathotype 40(BN1) in Sweden; even though the same pathotype has previously
been found in Poland it cannot directly be interpreted as the origin of the Swedish
isolate.
Recent progress of detection and diagnostic methods
Several collaborative research initiatives have been done during the last decade to
improve the detection and diagnostics methods available, e.g.;
• Euphresco project SENDO (Diagnostic methods for Synchytrium
endobioticum, especially for pathotype identification, 2012-2015)(
https://www.euphresco.net/projects/portfolio)
• Euphresco project SENDO D1 (Development of pathotype-specific PCR
tests for the identification of Synchytrium endobioticum pathotype 1(D1),
2013-2014) (https://www.euphresco.net/projects/portfolio)
• CORNET project SynTest (Establishment of a harmonized methodology
for testing the resistance of potato cultivars to potato wart disease
(Synchytrium endobioticum) in the EU, 2013-2015)
(http://www.ihar.edu.pl/cornet2.php)
https://www.euphresco.net/projects/portfoliohttps://www.euphresco.net/projects/portfoliohttp://www.ihar.edu.pl/cornet2.php
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
10/23
As a result of these efforts the standard describing the bioassays for pathotype
identification has been revised and different molecular methods has been
developed and validated as briefly described below.
Pathotype identification
The robustness and reproducibility of the Glynne-Lemmerzahl method for
pathotype identification was evaluated in five laboratories in Germany, Poland and
the Netherlands by Flath et al. (2014). For some pathotypes and potato cultivars
different results were found between laboratories and specific protocols. Further
interlaboratory tests of differential potato cultivars has also been performed within
the Euphresco-SENDO project and in the CORNET project SynTest (Flath et al.
2014; www.ihar.edu.pl/cornet2.php).
In 2017, the EPPO diagnostic standard for Synchytrium endobioticum, originally
published in 2003, was revised and the list of differential potato cultivars used for
pathotype identification was updated (EPPO, 2017a). This standard is, however,
still limited to distinguish between the pathotypes 1(D1), 2(G1), 6(O1) and 18(T1).
There is currently no agreed standard assay available to detect and describe other
pathotypes than the four most important ones. A method able to differentiate all
relevant pathotypes may facilitate both the detection and management of less
common pathotypes as well as the detection of new pathotypes.
Resistance screening using bio-assays are both labour and time intensive and
efforts have been placed into the development of molecular methods. A real-time
Taqman PCR assay was developed that can discriminate between pathotype 1(D1)
and other pathotypes (Bonants et al. 2015). The method is currently the only
molecular method described that can differentiate between the different pathotypes.
Still, the method is limited to discriminate pathotype 1(D1) from other pathotypes
and has not been validated on other pathotypes than 2(G1), 6(O1), 18(T1). In
addition, the method can only be used for diagnostic purposes if a positive result is
obtained since isolates of pathotype 1(D1), identified by a bioassay, from different
geographic origin display some genetic variation in the target marker and negative
results obtained may thus be false (Bonants et al. 2015; van de Vossenberg et al.
2018b). This has for example been found for an isolate of pathotype 1(D1) from
Sweden (van de Vossenberg et al. 2018b). Thus, the identification of pathotype
1(D1) isolates lacking the marker and the identification of other pathotypes is still
dependent on bioassays.
Development and validation of molecular methods for detection and
identification
Several molecular methods are available to identify and detect S. endobioticum,
e.g. conventional PCR amplification of the ITS region (Niepold and Stachewicz,
2004; van den Boogert et al. 2005), a real-time PCR approach to amplify ITS2
from soil and plant tissue (van Gent-Pelzer et al. 2010) and a real-time PCR assay
amplifying in tandem the SSU and the ITS1 from soil samples (Smith et al. 2014).
http://www.ihar.edu.pl/cornet2.php
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
11/23
Recently, van de Vossenberg et al. (2018b) published the results of a test
performance study aimed to generate validation data for molecular assays. All the
methods evaluated (van den Boogert et al. 2005; van Gent-Pelzer et al. 2010;
Bonants et al. 2015) performed equally on DNA extracted from warted potato
tissue. On samples of resting spore suspension, the assay by Gent-Pelzer et al.
(2010) was the best in terms of overall accuracy and analytical sensitivity and the
authors conclude this as the method of choice for identification of resting spores.
The EPPO diagnostics was revised in 2017 taking into account the development of
the molecular detection and diagnostics methods (EPPO, 2017a; van de
Vossenberg et al. 2018b).
Resistance in potato against different pathotypes
Genetic components of resistance
Several studies have been devoted to elucidate the genetic basis of the resistance of
potato against S. endobioticum. The progress in understanding has, however, been
limited both by the fact that different studies have used potato material with
different genetic background for the analysis, for example with different ploidy
level (i.e. the number of chromosomes), and because the resistance is based on
several genes (Obideigwu et al. 2014). Cultivated potato is normally tetraploid,
having four sets of each chromosome, but can also be diploid, having two sets of
chromosomes. The cultivated tetraploid potato also has a very complex inheritance
pattern making breeding for disease resistance complicated (Muthoni et al. 2015).
The resistance in potato against pathotype 1(D1) has been linked to one or two
dominant genes (e.g. Sen 1) (Hehl et al., 1999; Brugmans et al., 2006). It was thus
suggested that only one gene mainly control the resistance against this pathotype
(Groth et al. 2013). The resistance in potato against pathotype 1(D1) has thus been
regarded as a mainly qualitative trait resulting in either complete resistant or
susceptible reactions (Flath et al. 2014). However, later studies suggest that other
genes may also be involved in the resistance against pathotype 1(D1) (Obideigwu
et al. 2015). The conflicting results have been attributed to differences in ploidy
level of the potato genotypes used in the studies (Obidiegwu et al. 2015).
The resistance in potato against the new pathotypes observed after the 1940’s, e.g.
pathotype 2(G1), 6(O1) and 18(T1) appear nevertheless to be clearly linked to
multiple genes (Groth et al. 2013). No individual marker loci in itself could explain
the variation in resistance, but combined together they were found to result in a
significant reduction in disease severity (Groth et al. 2013). Some loci were only
linked to certain pathotypes while others were linked to several (Groth et al. 2013).
The involvement of multiple alleles for resistance results in a quantitative trait with
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
12/23
varying levels of resistance and susceptibility depending on the genes present in the
potato cultivar (Flath et al. 2014).
Whether the main resistance locus found (i.e. Sen1), clearly linked to the resistance
of pathotype 1(D1), is also involved in the resistance against the other pathotypes
has not been unanimously reported in the literature. Groth et al. (2013) state that
this locus does not seem to be effective against the pathotypes 2(G1), 6(O1) and
18(T1) while Obidiegwu et al. (2015), on the other hand, observed the opposite.
Again this is suggested to be a result of the tetraploid nature of potato and that
there are multiple resistance alleles at the same locus that differ between potato
families thus giving rise to different results in the studies conducted (Obidiegwu et
al. 2015). Recently however, Plich et al. (2018) found resistance gene sen1 to only
be linked to resistance against pathotype 1(D1).
The study by Plich et al. (2018) further found another broad spectrum resistance
gene (sen2), which provided resistance against all pathotypes tested (1(D1), 2(G1),
6(O1), 8(F1), 18(T1), 2(Ch1), 3(M1) and 39(P1)). The study was made on diploid
potato clones and the efficiency of the resistance gene needs to be confirmed in
tetraploid cultivated potato (Plich et al. 2018).
Breeding and resistant potato cultivars
Breeding for resistance in potato against S. endobioticum started some 100 years
ago and was successful in developing resistant cultivars against pathotype 1(D1)
(Obidiegwu et al. 2014), presumably due to the presence of a dominant resistance
gene and the dominance of one pathotype (e.g. Lellbach and Effmert, 1990). More
than 450 cultivars of potato resistant against this pathotype are available as listed
by the NPPO in the Netherlands (NVWA, 2018).
The breeding for resistance against the newer pathotypes reported after the 1940’s
has proven to be more difficult (Baayen et al. 2005 and references therein). Only
15-29 cultivars are listed as resistant against the new pathotypes 2(G1), 6(O1) and
18(T1) and only five potato cultivars are listed as resistant against all four of the
pathotypes by the Dutch NPPO (NVWA, 2018).
Studies indicate that resistance against pathotypes 2(G1), 6(O1) and 18(T1) may
frequently be inherited together, i.e. genetic markers for resistance against these
pathotypes frequently occur in combination (Ballvora et al. 2011; Groth et al.
2013). Markers for resistance against pathotype 1(D1), on the other hand, appear to
be independent from the other pathotypes, although some exceptions exist
(Ballvora et al. 2011; Groth et al. 2013; Obidiegwu et al. 2015). This pattern is,
however, not clearly observed in the potato cultivars listed by the Dutch NPPO and
for the pathotypes 2(G1), 6(O1) and 18(T1), about half of the listed resistant potato
cultivars were only demonstrated to be resistant against one of these pathotypes
(NVWA, 2018). Although, this lack of a pattern could potentially also be the result
of an uneven resistance screening intensity for the different pathotypes.
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
13/23
In a report to the Danish NPPO, Nielsen (2017) has collected information
regarding the reported resistance of different potato cultivars to different
pathotypes. Following the resistant classification of Langerfeld & Stachewicz
(1994) for cultivar testing the list includes; 162 cultivars resistant against pathotype
1(D1), 22 cultivars resistant against pathotype 6(O1), 18 cultivars resistant against
pathotype 2(G1), 15 cultivars resistant against pathotype 18(T1) and only two
cultivars resistant against pathotype 8(F1) (i.e. Otolia and Tivoli; Nielsen, 2017).
None of the potato cultivars is listed as resistant against all 5 pathotypes but more
than half of the cultivars resistant against the new pathotypes are resistant against
more than one of them.
However, not all cultivars have been tested against all pathotypes, e.g. the low
number of potato cultivars reported to be resistant against pathotypes 8(F1) may
also be due to the low number of potato cultivars specifically tested against this
pathotype (Nielsen, 2017). Nevertheless, Nielsen (2017) further states that potato
varieties described as resistant to pathotype 18(T1) are also generally considered to
be resistant to pathotype 8(F1) (Nielsen (2017) citing personal communication with
Leeuwen, Flath, and Przetakiewicz) or the difference between them may be very
small (Nielsen (2017) citing personal communication with Boerma).
Potato cultivars verified to be resistant against pathotype 40(BN1) are Megusta,
Otolia, Saphir, Ulme and Nicola (J. Przetakiewicz, pers.comm.).
Management options and perspectives
Epidemiology and management
S. endobioticum is an obligate biotroph only able to extract nutrients from living
host tissues. Potato (Solanum tuberosum) is the main host, although other Solanum
species (e.g. S. dulcamara and S. nigrum), tomato (Lycopersicon esculentum) as
well as species from other genera have been successfully infected in laboratory
experiments (Weiss, 1925; Hampson, 1993). Any contribution of other species than
potato in the epidemiology of the disease has yet to be confirmed (Arora and
Sharma, 2014).
The main means of spread of the pathogen is considered to be via seed potato
tubers (Franc 2007). Symptoms may be small and can thus be overlooked in
infected fields or may take weeks to month to become visible on infected potato
tubers. The pathogen can also spread via the dispersal of winter sporangia in soil
attached to tubers and machinery or in soil of potted ornamental plants (Franc
2007; Obidiegwu et al. 2014). Other means of spread listed in the literature
includes spread via manure, earth worms, windblown dust and run off water
(Obidiegwu et al. 2014 and references therein). In Denmark, the pathogen was
suggested to have been spread by wash water from a starch potato industry
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
14/23
(Nielsen, 2017). The local dispersal capacity is very limited and the zoospores
themselves for example are only capable of limited spread in the soil, up to 5 cm,
and survival is limited to 1-2 h (Weiss, 1925; Franc, 2007).
The pathogen is however extremely resilient due to its durable winter sporangia.
Winter sporangia have been found to survive composting for 12 days at 60-65C
and for longer time periods at lower temperatures (Steinmöller et al. 2012). Winter
sporangia were also found to survive 90 min at 70C (i.e. pasteurisation) and 8 h at
80C in a water bath and at 90C in a dry oven (Steinmöller et al. 2012).
Furthermore, investigations of the survival of S. endobioticum in sewage sludge
using quantitative examinations with isolated and dried resting sporangia and
different types of sewage sludge showed that viable resting sporangia (around 30-
40%) was found after a 2h treatment at 140C (4bar) (UBA, 2015). Storage of the
sewage sludge reduced the proportion of viable resting sporangia, but viability
rates differed between sewage sludge type and storage conditions and viable
sporangia were still found after 5 month storage (UBA, 2015).
Crop rotation decreases the risk for build-up of sporangia in the field and thereby
reduces the risk for infections. However, crop rotation can also fail to efficiently
control S. endobioticum since it has dormant structures that can survive in the soil
for very long periods and a very low inoculum density is sufficient to induce
disease (Fiers et al. 2012). Under ideal conditions very low levels of inoculum have
been found to induce disease and
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
15/23
measures to prevent further spread must be implemented as outlined in Council
Directive 69/464/EEC on control of potato wart disease. In short, cultivation of
potato is prohibited in fields found to be infested by S. endobioticum and in a safety
zone surrounding the infested field, potato cultivation is allowed only if cultivars
used are sufficiently resistant to the pathotype present to prevent secondary
infection.
In many ways the current measures appear to have been effective. Although the
pathogen has been present in Europe for more than a hundred years the
geographical distribution of the pathogen is still restricted in most countries where
it is found. Yet, the pathogen is still discovered in new countries and locations and
new pathotypes that have broken the resistance of some of the cultivated potato
varieties used are discovered (e.g. Çakir et al. 2005, 2009; Przetakiewicz, 2015b).
Prevention of spread
In Council Directive 69/464/EEC it is stated that;
“A potato variety shall be regarded as being resistant to a particular race of
Synchytrium endobioticum when it reacts to contamination by the pathogenic agent
of that race in such a way that there is no danger of secondary infection.”.
As argued in Baayen et al. (2005) this means that complete resistance is not
required but rather that no further spread of the infection should be possible in the
current crop with summer sporangia or the following crop with surviving winter
sporangia. Such secondary spread in effect will also depend on the build-up of
sporangia, the disease threshold, i.e. density of sporangia needed for infection of a
certain cultivar, and different abiotic factors (Baayen et al. 2005).
This gives rise to two aspects to consider; i) what level of resistance is required and
ii) how can it be determined.
The resistance against the different pathotypes is often displayed as a quantitative
trait with varying levels of resistance and susceptibility (Flath et al. 2014). It is
however not clearly defined where the level of resistance in potato cultivars should
be placed in order to ensure the elimination of further spread (Langerfeld &
Stachewicz 1994; Baayen et al. 2005). Further, there is currently no agreed
guidance on how to assess the level of resistance of different potato cultivars. The
resistance tests described in the EPPO standard PM 7/28 is for pathotype
identification and the revised version published in 2017 does not include any
details regarding the classification of the degree of resistance (c.f. EPPO, 2004). A
new standard providing guidance on testing of potato varieties to assess the
resistance to S. endobioticum is, however, under development at EPPO with the
goal to finalize a draft in 2019 (EPPO 2017c; EPPO 2018b).
Nevertheless, most resistance screening appear to be done following the scheme by
Langerfeld & Stachewicz (1994) where five reaction types are described (as
summarized by Obidiegwu et al 2014):
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
16/23
• Extremely resistant (R1) = early defence necrosis; no visible sorus1 formation
• Resistant (R1) = late defence necrosis; single necrotic sori visible
• Weakly resistant (R2) = very late defence necrosis; up to five non-necrotic sori
• Slightly susceptible (S1) = scattered infections; sorus fields, sprout can be malformed
• Extremely susceptible (S2) = dense infection fields, numerous ripe sori and sorus fields, predominant tumor formation
Potato cultivars categorised as either R1 or R2 appear to generally be considered as
resistant cultivars (e.g. Nielsen, 2017). Cultivars with this level of resistance are
assumed to fulfil the requirement of Council Directive 69/464/EEC.
The Netherlands also appear to use another scale to identify the resistance level
required for cultivation of so called “prevention areas”, i.e. areas outside the safety
zone, and for such areas a lower level of resistance is allowed (Baayen et al. 2005;
Nielsen 2017). In the Netherlands, studies indicate that a field resistance ≥7, on a
scale to 9, would adequately prevent secondary infection in tests done on pathotype
1(D1) and 6(O1) (Baayen et al. 2005).
Resistance screening of different potato cultivars against the pathotypes is reported
to currently be done mainly in the laboratory using the same methods applied for
pathotype description, i.e. the Glynne-Lemmerzahl method or the Spieckermann
method (Obidiegwu et al. 2014; Nielsen, 2017). Field tests does not appear to be
commonly used as environmental variation may affect the reliability (Obidiegwu et
al. 2014). Baayen et al. (2005), nevertheless, showed that field tests could provide
stable results in tests done on pathotype 1(D1) and 6(O1) when environmental
variation was statistically corrected.
Emergence of new pathotypes
The emergence of new pathotypes is difficult to manage (Obidiegwu et al. 2014).
According to Bojnansky (1984) new pathotypes frequently originate and occur in
gardens and small size plots where potatoes are commonly grown for own needs or
in areas where there is a high probability of direct transmission by e.g. seed
potatoes and contaminated tools. Many of the new pathotypes has also been
associated with areas with favourable climatic conditions (Bojnansky 1984;
Przetakiewicz 2015b). Pathotype 39(P1) was, for example, found in a small garden
potato plot in a rainy mountainous area where potatoes were cultivated without
crop rotations (Przetakiewicz 2015b).
1 A sorus (plural sori) is a clusters of sporangia.
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
17/23
It is also hypothesised that new virulent pathotypes develop on potato cultivars that
are not completely resistant (Melnik 1998; Plich et al. (2018) citing Malec (1974)).
Studies suggest that if the pathogen is able to complete its life cycle, including the
sexual reproduction cycle, on partially resistant cultivars the virulence may
increase (Melnik 1998 and references therein). Cultivation of cultivars with
incomplete resistance may select for new pathotypes that display slightly different
resistant profiles, e.g. the development of pathotype 39(P1) and 40(NB1) has for
example been suggested to originate from the Polish pathotype 2(Ch1)
(Przetakiewicz 2015b; European Commission 2014).
Such a shift in phenotype is further supported by the recently published article Van
de Vossenberg et al. (2018a). This study also shows that this shift from one
pathotype to another can be a very rapid process as an isolate with a pathotype
1(D1) phenotype changed into a pathotype 6(O1) phenotype after only two
multiplications on a partially resistant potato cultivar. The authors also observed an
increased diversity of the isolate and suggest that the changed virulence profile was
the result of a selection of virulent genotypes already present among the genotypes
present in the isolate (Van de Vossenberg et al. 2018a).
Such potential change in virulence due to the selection of the pathogen population
needs to be considered when developing control strategies (Van de Vossenberg et
al. 2018a). Melnik (1998) state the necessity to define the resistance of new
cultivars and to breed cultivars with high resistance to prevent the development of
the pathogen. When breeding potato for resistance for example it may be advisable
to combine several resistance genes to enhance the durability of the resistance
(Plich et al. 2018).
Descheduling of previously infected fields
For a general background of the descheduling procedure of previously infected
fields see McNamara and Smith (1998).
In Council Directive 69/464/EEC, Article 6, it is stated that; “The Member States
shall revoke the measures taken to control Potato Wart Disease or to prevent it
from spreading only if Synchytrium endobioticum is no longer found to be
present.”. The specific requirements for revoking the demarcation of the infected
fields or ‘descheduling’ previously scheduled plots are not given in the Council
Directive.
However, a guidance is given in the EPPO standard describing the procedure for
descheduling plots previously infested by S. endobioticum (PM 3/59) which was
revised in 2017 (EPPO, 2017b). The standard includes a procedure to support a
complete or partial descheduling of plots previously infested by S. endobioticum.
Plots where the last detection of the pathogens was done > 50 years ago and where
no susceptible crops have been grown can be completely descheduled without any
further tests. Plots where the last detection was done > 20 years ago can be
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
18/23
completely descheduled if bioassays performed on specific number of soil samples
are negative.
There is also a procedure described to support a partial descheduling after >10
years or after >5 years (if soil are treated or not conducive) also based on negative
bioassays of a specific number of soil samples. Partially descheduled plots may
then be used for cultivation of resistant potato cultivars.
Authors
This report was prepared by the Unit for Risk Assessment of Plant Pests at the
Swedish University of Agricultural Sciences:
Johanna Boberg, Dept. of Forest Mycology and Plant Pathology, PO Box 7026,
SE-750 07 Uppsala, Sweden. Visiting address: Almas allé 5, E-mail:
Niklas Björklund, Dept. of Ecology, Swedish University of Agricultural Sciences,
P.O. Box 7044, S-750 07 Uppsala, Sweden. Delivery address: Ullsväg 16, E-mail:
The content of this report was reviewed by:
Björn Andersson, Forest Mycology and Plant Pathology, Swedish University of
Agricultural Sciences, Uppsala
Erland Liljeroth, Department of Plant Protection Biology, Swedish University of
Agricultural Sciences, Alnarp
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
19/23
References
Arora, R.K. & Sharma, S. (2014). Pre and post harvest diseases of potato and their
management. In: Future Challenges in Crop Protection Against Fungal Pathogens, Fungal
Biology, (eds. Goyal, A. and Manoharachary, C.), Springer, New York, 149-183
Baayen, R. P., Bonthuis, H., Withagen, J. C. M., Wander, J. G. N., Lamers, J. L., Meffert, J.
P., ... & Van den Boogert, P. H. J. F. (2005). Resistance of potato cultivars to Synchytrium
endobioticum in field and laboratory tests, risk of secondary infection, and implications for
phytosanitary regulations. EPPO Bulletin, 35(1), 9-23.
Baayen, R. P., Cochius, G., Hendriks, H., Meffert, J. P., Bakker, J., Bekker, M., ... & Van
Leeuwen, G. C. M. (2006). History of potato wart disease in Europe–a proposal for
harmonisation in defining pathotypes. European Journal of Plant Pathology, 116(1), 21-31.
Ballvora, A., Flath, K., Lübeck, J., Strahwald, J., Tacke, E., Hofferbert, H. R., & Gebhardt,
C. (2011). Multiple alleles for resistance and susceptibility modulate the defense response
in the interaction of tetraploid potato (Solanum tuberosum) with Synchytrium endobioticum
pathotypes 1, 2, 6 and 18. Theoretical and applied genetics, 123(8), 1281-1292.
Bojnansky, V. (1984). Potato wart pathotypes in Europe from the ecological point of
view. EPPO Bulletin, 14(2), 141-146.
Bonants PJM, van Gent-Pelzer MPE, van Leeuwen GCM & van der Lee TAJ (2015) A
real-time TaqMan PCR assay to discriminate between pathotype 1(D1) and non-pathotype
1(D1) isolates of Synchytrium endobioticum. European Journal of Plant Pathology 143,
495–506.
Browning, I. A. (1995). A comparison of laboratory and field reactions of a range of potato
cultivars to infection with Synchytrium endobioticum (Schilb.) Perc. Potato research, 38(3),
281-289.
Brugmans, B., Hutten, R. G., Rookmaker, A. N. O., Visser, R. G., & van Eck, H. J. (2006).
Exploitation of a marker dense linkage map of potato for positional cloning of a wart
disease resistance gene. Theoretical and applied genetics, 112(2), 269-277.
Busse, F., Bartkiewicz, A., Terefe-Ayana, D., Niepold, F., Schleusner, Y., Flath, K., ... &
Hofferbert, H. R. (2017). Genomic and transcriptomic resources for marker development in
Synchytrium endobioticum, an elusive but severe potato pathogen. Phytopathology, 107(3),
322-328.
Çakir, E. (2005). First report of potato wart disease in Turkey. New disease report, Plant
Pathology 54, 584.
Çakır, E., Van Leeuwen, G. C. M., Flath, K., Meffert, J. P., Janssen, W. A. P., & Maden, S.
(2009). Identification of pathotypes of Synchytrium endobioticum found in infested fields in
Turkey. EPPO bulletin, 39(2), 175-178.
Çakir, E., & Demirci, F. (2017) A new pathotype of Synchytrium endobioticum in Turkey:
Pathotype 2. BİTKİ KORUMA BÜLTENİ 57(4) : 415 – 422. Doi:
10.16955/bitkorb.340441
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
20/23
EPPO (2004). Diagnostic protocols for regulated pests, Synchytrium endobioticum. PM
7/28(1). EPPO Bulletin, 34:213-218.
EPPO (2017a). EPPO diagnostics PM 7/28(2) Synchytrium endobioticum. EPPO Bulletin,
47, 420-440.
EPPO (2017b). EPPO phytosanitary procedures PM 3/59(3) Synchytrium endobioticum:
descheduling of previously infested plots. EPPO Bulletin 47, 366-368.
EPPO (2017c). PM 9/5 (2) Synchytrium endobioticum. Bulletin OEPP/EPPO Bulletin
(2017) 47 (3), 511–512. https://onlinelibrary.wiley.com/doi/epdf/10.1111/epp.12440
EPPO (2018a) EPPO Global Database (available online). https://gd.eppo.int [accessed
2018-08-24]
EPPO (2018b). 24th meeting of the panel on phytosanitary measures for potato, Paris,
2018-02-21/23. https://www.eppo.int/MEETINGS/2018_meetings/potato_phytomeasures
European Commission (2014). Final report of an audit carried out in Poland from 04
November 2014 to 14 November 2014 in order to evaluate the plant health controls applied
in the potato sector. European Commissions - Directorate- general for health and food
safety. Ref. Ares(2015)3021859 - 17/07/2015. Retrieved from
http://ec.europa.eu/food/fvo/act_getPDF.cfm?PDF_ID=11789
Fiers, M., Edel-Hermann, V., Chatot, C., Le Hingrat, Y., Alabouvette, C., & Steinberg, C.
(2012). Potato soil-borne diseases. A review. Agronomy for Sustainable Development,
32(1), 93-132.
Fitopatologii, Z. (2016). Raport na temat identyfikacji izolatów grzyba S. endobioticum w
Polsce. Instytut Hodowli i Aklimatyzacji Roslin (IHAR), p. 1-3. Retrieved from
http://pw.ihar.edu.pl/assets/Uploads/Raport-po-2-latach-PW-4.1.2-S.-endobioticum.pdf
Flath, K., Przetakiewicz, J., Rijswick, P. C. J., Ristau, V., & Leeuwen, G. C. M. (2014).
Interlaboratory tests for resistance to Synchytrium endobioticum in potato by the Glynne‐
Lemmerzahl method. EPPO Bulletin, 44(3), 510-517.
Franc, G. (2007). Potato wart. Online. APSnet Features. doi: 10.1094/APSnetFeature-2007-
0607
Gagnon, M. C., van der Lee, T. A., Bonants, P. J., Smith, D. S., Li, X., Lévesque, C. A., &
Bilodeau, G. J. (2016). Development of polymorphic microsatellite loci for potato wart
from next-generation sequence data. Phytopathology, 106(6), 636-644.
Groth, J., Song, Y., Kellermann, A., & Schwarzfischer, A. (2013). Molecular
characterisation of resistance against potato wart races 1, 2, 6 and 18 in a tetraploid
population of potato (Solanum tuberosum subsp. tuberosum). Journal of applied genetics,
54(2), 169-178.
Hammarlund, C., 1915. Försök med utrotning av potatiskräfta. (Synchytrium endobioticum
PERC.). Meddelande N:r 127 från Centralanstalten för försöksväsendet på
jordbruksområdet. Botaniska avdelningen N:r 11.
https://onlinelibrary.wiley.com/doi/epdf/10.1111/epp.12440https://gd.eppo.int/http://ec.europa.eu/food/fvo/act_getPDF.cfm?PDF_ID=11789http://pw.ihar.edu.pl/assets/Uploads/Raport-po-2-latach-PW-4.1.2-S.-endobioticum.pdf
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
21/23
Hampson, M.C. (1992). A bioassay for Synchytrium endobioticum using micropropagated
potato plantlets. Canadian Journal of Plant Pathology, 14(4), 289-292.
Hampson, M. C. (1993). History, biology and control of potato wart disease in Canada.
Canadian Journal of Plant Pathology, 15(4), 223-244.
Hartman, R. E. (1955). Potato wart eradication program in Pennsylvania. American Journal
of Potato Research, 32(9), 317-326.
Hehl, R., Faurie, E., Hesselbach, J., Salamini, F., Whitham, S., Baker, B., & Gebhardt, C.
(1999). TMV resistance gene N homologues are linked to Synchytrium endobioticum
resistance in potato. Theoretical and applied genetics, 98(3-4), 379-386.
Khiutti, A., Afanasenko, O., Antonova, O., Shuvalov, O., Novikova, L., Krylova, E., ... &
Gavrilenko, T. (2012). Characterization of resistance to Synchytrium endobioticum in
cultivated potato accessions from the collection of Vavilov Institute of Plant Industry. Plant
breeding, 131(6), 744-750.
Laginova, M.. (2017). Standpoint about the spread of potato wart disease in Bulgaria
(Synchytrium endobioticum); pathotypes identification and testing of potato varities for
resistance. Summary in English. Zenodo. Retrieved from
http://doi.org/10.5281/zenodo.830435
Langerfeld E, Stachewicz H (1994) Assessment of varietal reaction to potato wart
(Synchytrium endobioticum) in Germany. EPPO Bulletin 24:793–798
Lellbach, H., & Effmert, M. (1990). Results of diallel analysis of the genetics of resistance
to Synchytrium endobioticum (Schilb.) Perc., pathotype 1 (D1) of potato (Solanum
tuberosum L.). Potato Research, 33(2), 251-256.
McNamara, D. G., & Smith, I. M. (1998). National control measures for Synchytrium
endobioticum. EPPO Bulletin, 28(4), 507-511.
Melin, G., & Nordin, K. (1996). Potatiskräfta. Faktablad om växtskydd – Jordbruk. 55 J.
Sveriges lantbruksuniversitet.
Melnik PA. (1998). Wart disease of potato, Synchytrium endobioticum (Schilbersky)
Percival. In: EPPO technical documents, Paris, pp 880–884.
Muthoni, J., Kabira, J., Shimelis, H., & Melis, R. (2015). Tetrasomic inheritance in
cultivated potato and implications in conventional breeding. Australian Journal of Crop
Science, 9(3), 185.
Nielsen, B. J. (2017) Redegørelse for kategorisering og bestemmelse på europæisk plan af
kartoffelsorters resistens overfor Synchytrium endobioticum (kartoffelbrok). Report from
DCA – Nationalt Center for Jordbrug og Fødevarer. Retrieved from
https://pure.au.dk/ws/files/114706744/20170309_Besvarelse_kartoffelbrok_resistens.pdf
Niepold, F., & Stachewicz, H. (2004). PCR-detection of Synchytrium endobioticum
(Schub.) Perc./PCR-Nachweis von Synchytrium endobioticum (Schilb.) Perc. Zeitschrift für
Pflanzenkrankheiten und Pflanzenschutz/Journal of Plant Diseases and Protection, 313-321.
http://doi.org/10.5281/zenodo.830435https://pure.au.dk/ws/files/114706744/20170309_Besvarelse_kartoffelbrok_resistens.pdf
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
22/23
Nordin, K. & Kvist, M (2008). Potatiskräfta. Jordbruksinformation 5 – 2008.
Jordbruksverket. Retrieved from:
http://www2.jordbruksverket.se/webdav/files/SJV/trycksaker/Pdf_jo/jo08_5.pdf
NVWA, (2018), List of all potato varieties officially registered as resistant to Synchytrium
endobioticum in 2018. Netherlands Food and Consumer Product Safety Authority (NVWA)
– NPPO of the Netherlands. Retrieved from
http://www.lansstyrelsen.se/VastraGotaland/Sv/lantbruk-och-landsbygd/Vaxtodling-
vaxtskydd/Sidor/Karantanskadegorare.aspx
Obidiegwu, J. E., Flath, K., & Gebhardt, C. (2014). Managing potato wart: a review of
present research status and future perspective. Theoretical and applied genetics, 127(4),
763-780.
Obidiegwu, J. E., Sanetomo, R., Flath, K., Tacke, E., Hofferbert, H. R., Hofmann, A., ... &
Gebhardt, C. (2015). Genomic architecture of potato resistance to Synchytrium
endobioticum disentangled using SSR markers and the 8.3 k SolCAP SNP genotyping
array. BMC genetics, 16(1), 38.
Plich, J., Przetakiewicz, J., Śliwka, J., Flis, B., Wasilewicz-Flis, I., & Zimnoch-Guzowska,
E. (2018). Novel gene Sen2 conferring broad-spectrum resistance to Synchytrium
endobioticum mapped to potato chromosome XI. Theoretical and Applied Genetics, 1-11.
Przetakiewicz, J. (2010). Resistance of Polish cultivars of potato to virulent pathotypes of
Synchytrium endobioticum (Schilb.) Per.: 2 (Ch1) and 3 (M1). Biuletyn Instytutu Hodowli i
Aklimatyzacji Roślin, (257/258), 207-214.
Przetakiewicz, J. (2014). First report of Synchytrium endobioticum (potato wart disease)
pathotype 18 (T1) in Poland. Plant Disease, 98(5), 688-688.
Przetakiewicz, J. (2015a). The Viability of Winter Sporangia of Synchytrium endobioticum
(Schilb.) Perc. from Poland. Am. J. Potato Res. 92:704-708
Przetakiewicz, J. (2015b). First report of new pathotype 39 (P1) of Synchytrium
endobioticum causing potato wart disease in Poland. Plant Disease, 99(2), 285-285.
UBA, (2015), Risikoanalyse der bodenbezogenen Verwertung kommunaler Klärschlämme
unter Hygieneaspekten, TEXTE 96/2015, Umweltforschungsplan des Bundesministeriums
für Umwelt, Naturschutz, Bau und Reaktorsicherheit (UBA), Forschungskennzahl 3711 71
240 UBA-FB 002139, Dessau-Roßlau, Retrived from
https://www.umweltbundesamt.de/publikationen/risikoanalyse-der-bodenbezogenen-
verwertung
Schlenzig, A. (2008). An update on potato wart disease. In The Dundee Conference. Crop
Protection in Northern Britain, 2008, Dundee, UK, 26-27 February 2008 (pp. 211-216).
The Association for Crop Protection in Northern Britain. Retrieved from
https://www.cabdirect.org/cabdirect/FullTextPDF/2014/20143111028.pdf
Smith, D. S., Rocheleau, H., Chapados, J. T., Abbott, C., Ribero, S., Redhead, S. A., ... &
De Boer, S. H. (2014). Phylogeny of the genus Synchytrium and the development of
TaqMan PCR assay for sensitive detection of Synchytrium endobioticum in soil.
Phytopathology, 104(4), 422-432.
http://www2.jordbruksverket.se/webdav/files/SJV/trycksaker/Pdf_jo/jo08_5.pdfhttp://www.lansstyrelsen.se/VastraGotaland/Sv/lantbruk-och-landsbygd/Vaxtodling-vaxtskydd/Sidor/Karantanskadegorare.aspxhttp://www.lansstyrelsen.se/VastraGotaland/Sv/lantbruk-och-landsbygd/Vaxtodling-vaxtskydd/Sidor/Karantanskadegorare.aspxhttps://www.umweltbundesamt.de/publikationen/risikoanalyse-der-bodenbezogenen-verwertunghttps://www.umweltbundesamt.de/publikationen/risikoanalyse-der-bodenbezogenen-verwertunghttps://www.cabdirect.org/cabdirect/FullTextPDF/2014/20143111028.pdf
Synchytrium endobioticum – pathotypes, resistance of Solanum tuberosum and management
23/23
Stachewicz H (1978). Evidence of a new biotype of the potato wart pathogen Synchytrium
endobioticum (Schilb.) Perc. in the German Democratic Republic. [Nachweis eines neuen
Biotypen des Kartoffelkrebserregers Synchytrium endobioticum (Schilb.) Perc. in der
DDR]. Nachrichtenblatt fur den Pflanzenschutz in der DDR 32.
Steinmöller, S., Bandte, M., Büttner, C., & Müller, P. (2012). Effects of sanitation
processes on survival of Synchytrium endobioticum and Globodera rostochiensis. European
journal of plant pathology, 133(3), 753-763.
Swedish Board of Agriculture (2018)
www.jordbruksverket.se/amnesomraden/odling/vaxtskydd/karantanskadegorare/skadegorar
epajordbruksgrodor/potatiskrafta.4.207049b811dd8a513dc8000681.html [accessed
September 17, 2018]
Van den Boogert, P. H. J. F., van Gent-Pelzer, M. P. E., Bonants, P. J. M., De Boer, S. H.,
Wander, J. G. N., Lévesque, C. A., ... & Baayen, R. P. (2005). Development of PCR-based
detection methods for the quarantine phytopathogen Synchytrium endobioticum, causal
agent of potato wart disease. European Journal of Plant Pathology, 113(1), 47-57.
Van de Vossenberg, B.T.L.H., Brankovics, B., Nguyen, H.D.T., van Gent-Pelzer, M.P.E.,
Smith, D., Dadej, K., Przetakiewicz, Kreuze, J.K., Boerma, M., van Leuwen, G.C.M.,
Lévesque, C.A., van der Lee, T.A.J. (2018a). The linear mitochondrial genome of the
quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history
of an obligate biotrophic plant pathogen. BMC Evolutionary Biology 18:136.
https://doi.org/10.1186/s12862-018-1246-6
van de Vossenberg, B., Westenberg, M., Adams, I., Afanasenko, O., Besheva, A., Boerma,
M., ... & Heungens, K. (2018b). Euphresco Sendo: An international laboratory comparison
study of molecular tests for Synchytrium endobioticum detection and identification.
European Journal of Plant Pathology, 1-10.
van Gent-Pelzer, M. P., Krijger, M., & Bonants, P. J. (2010). Improved real-time PCR
assay for detection of the quarantine potato pathogen, Synchytrium endobioticum, in zonal
centrifuge extracts from soil and in plants. European journal of plant pathology, 126(1),
129.
Weiss, F. (1925) The conditions of infection in potato wart. American Journal of Botany,
12:413-443.
https://doi.org/10.1186/s12862-018-1246-6
SummaryBackground and assignmentDescription of Synchytrium endobioticumLife cycleGeographical distributionDifferent pathotypesSynchytrium endobioticum in SwedenGenetic components of virulenceRecent progress of detection and diagnostic methods
Resistance in potato against different pathotypesGenetic components of resistanceBreeding and resistant potato cultivars
Management options and perspectivesEpidemiology and managementResistant potato cultivars and Council Directive 69/464/EECDescheduling of previously infected fields
AuthorsReferences